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The Journal of Neuroscience, October 1, 2002, 22(19):8633-8646

Circuits for Local and Global Signal Integration in Primary Visual Cortex

Alessandra Angelucci¹, Jonathan B. Levitt², Emma J. S. Walton³, Jean-Michel Hupé⁴, Jean Bullier⁴, and Jennifer S. Lund¹

¹ Department of Ophthalmology and Visual Science, Moran Eye Center, University of Utah, Salt Lake City, Utah 84132, ² Department of Biology, City College of the City University of New York, New York, New York 10031, ³ Department of Visual Sciences, Institute of Ophthalmology, University College London, London EC1V 9EL, United Kingdom, and ⁴ Centre de Recherche Cerveau et Cognition, Centre National de la Recherche Scientifique-Unité Propre de Recherche Unité Mixte de Recherche 5549, Université Paul Sabatier, Toulouse 31062, France

Contrast-dependent changes in spatial summation and contextual modulation of primary visual cortex (V1) neuron responses to stimulation of their receptive field reveal long-distance integration of visual signals within V1, well beyond the classical receptive field (cRF) of single neurons. To identify the cortical circuits mediating these long-distance computations, we have used a combination of anatomical and physiological recording methods to determine the spatial scale and retinotopic logic of intra-areal V1 horizontal connections and inter-areal feedback connections to V1. We have then compared the spatial scales of these connectional systems to the spatial dimensions of the cRF, spatial summation field (SF), and modulatory surround field of macaque V1 neurons. We find that monosynaptic horizontal connections within area V1 are of an appropriate spatial scale to mediate interactions within the SF of V1 neurons and to underlie contrast-dependent changes in SF size. Contrary to common beliefs, these connections cannot fully account for the dimensions of the surround field. The spatial scale of feedback circuits from extrastriate cortex to V1 is, instead, commensurate with the full spatial range of center-surround interactions. Thus these connections could represent an anatomical substrate for contextual modulation and global-to-local integration of visual signals. Feedback projections connect corresponding and equal-sized regions of the visual field in striate and extrastriate cortices and cover anisotropic parts of visual space, unlike V1 horizontal connections that are isotropic in the macaque. V1 isotropic connectivity demonstrates that anisotropic horizontal connections are not necessary to generate orientation selectivity. Anisotropic feedback connections may play a role in contour completion.

Key words: primary visual cortex; extrastriate cortex; feedback connections; lateral connections; surround modulation; macaque

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Copyright © 2002 Society for Neuroscience  0270-6474/02/22198633-14$05.00/0

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